Different types of nsP3-containing protein complexes in sindbis virus-infected cells

Journal of Virology

Volumn 82, Issue 20, 2008, Pages 10088-10101

  Gorchakov, Rodion ^a   Garmashova, Natalia ^a   Frolova, Elena ^a   Frolov, Ilya ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DETERGENT; DOUBLE STRANDED RNA; HEAT SHOCK COGNATE PROTEIN 70; NEUROENDOCRINE SPECIFIC PROTEIN; PROTEIN G3BP1; PROTEIN G3BP2; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA; Y BOX BINDING PROTEIN 1; DNA DIRECTED RNA POLYMERASE; FLUORESCENT DYE; HYBRID PROTEIN; MULTIPROTEIN COMPLEX; NSP3 PROTEIN, VIRUS; RNA BINDING PROTEIN;

ALPHA VIRUS; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL NUCLEUS; CELL ORGANELLE; CELL STRAIN BHK; COMPLEX FORMATION; CONTROLLED STUDY; CYTOSKELETON; CYTOSOL; ENDOSOME; GENETIC CONSERVATION; INTRACELLULAR TRANSPORT; INVERTEBRATE; MAMMAL CELL; MOSQUITO; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN RNA BINDING; PROTEIN TRANSPORT; RNA SYNTHESIS; RNA VIRUS INFECTION; SINDBIS VIRUS; SOLUBILIZATION; VERTEBRATE; VIRUS CELL INTERACTION; VIRUS REPLICATION; ANIMAL; CELL LINE; CRICETULUS; GENETICS; HAMSTER; HUMAN; METABOLISM; PATHOGENICITY; VIRUS INFECTION;

HEXAPODA; INVERTEBRATA; MAMMALIA; SINDBIS VIRUS; VERTEBRATA;

ALPHAVIRUS INFECTIONS; ANIMALS; CELL LINE; CRICETINAE; CRICETULUS; CULICIDAE; DNA-DIRECTED RNA POLYMERASES; FLUORESCENT DYES; HUMANS; MULTIPROTEIN COMPLEXES; RECOMBINANT FUSION PROTEINS; RNA, DOUBLE-STRANDED; RNA, VIRAL; RNA-BINDING PROTEINS; SINDBIS VIRUS; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 53749083590     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01011-08     Document Type: Article

References (67)

1. Anderson, P., and N. Kedersha. 2006. RNA granules. J. Cell Biol. 172:803-808.
2. Atasheva, S., N. Garmashova, I. Frolov, and E. Frolova. 2008. Venezuelan equine encephalitis virus capsid protein inhibits nuclear import in mammalian but not in mosquito cells. J. Virol. 82:4028-4041.
3. Atasheva, S., R. Gorchakov, R. English, I. Frolov, and E. Frolova. 2007. Development of Sindbis viruses encoding nsP2/GFP chimeric proteins and their application for studying nsP2 functioning. J. Virol. 81:5046-5057.
4. Barton, D. J., D. L. Sawicki, and S. G. Sawicki. 1990. Association of alpha-virus replication with the cytoskeletal framework and transcription in vitro in the absence of membranes, p. 75-79. In M. A. Brinton and F. X. Heinz (ed.), New aspects of positive-strand RNA viruses. American Society for Microbiology, Washington, DC.
5. Barton, D. J., S. G. Sawicki, and D. L. Sawicki. 1991. Solubilization and immunoprecipitation of alphavirus replication complexes. J. Virol. 65:1496-1506.
6. Beck, J., and M. Nassal. 2003. Efficient Hsp90-independent in vitro activation by Hsc70 and Hsp40 of duck hepatitis B virus reverse transcriptase, an assumed Hsp90 client protein. J. Biol. Chem. 278:36128-36138.
7. Castorena, K. M., S. A. Weeks, K. A. Stapleford, A. M. Cadwallader, and D. J. Miller. 2007. A functional heat shock protein 90 chaperone is essential for efficient flock house virus RNA polymerase synthesis in Drosophila cells. J. Virol. 81:8412-8420.
8. Connor, J. H., M. O. McKenzie, G. D. Parks, and D. S. Lyles. 2007. Antiviral activity and RNA polymerase degradation following Hsp90 inhibition in a range of negative strand viruses. Virology 362:109-119.
9. Cristea, I. M., J. W. Carroll, M. P. Rout, C. M. Rice, B. T. Chait, and M. R. MacDonald. 2006. Tracking and elucidating alphavirus-host protein interactions. J. Biol. Chem. 281:30269-30278.
10. Dal Canto, M. C., and S. G. Rabinowitz. 1981. Central nervous system demyelination in Venezuelan equine encephalomyelitis infection. J. Neurol. Sci. 49:397-418.
11. De, I., C. Fata-Hartley, S. G. Sawicki, and D. L. Sawicki. 2003. Functional analysis of nsP3 phosphoprotein mutants of Sindbis virus. J. Virol. 77:13106-13116.
12. Fayzulin, R., and I. Frolov. 2004. Changes of the secondary structure of the 5′ end of the Sindbis virus genome inhibit virus growth in mosquito cells and lead to accumulation of adaptive mutations. J. Virol. 78:4953-4964.
13. Friedman, R. M., J. G. Levin, P. M. Grimley, and I. K. Berezesky. 1972. Membrane-associated replication complex in arbovirus infection. J. Virol. 10:504-515.
14. Frolova, E., R. Gorchakov, N. Garmashova, S. Atasheva, L. A. Vergara, and I. Frolov. 2006. Formation of nsP3-specific protein complexes during Sindbis virus replication. J. Virol. 80:4122-4134.
15. Frolova, E. I., R. Z. Fayzulin, S. H. Cook, D. E. Griffin, C. M. Rice, and I. Frolov. 2002. Roles of nonstructural protein nsP2 and alpha/beta interferons in determining the outcome of Sindbis virus infection. J. Virol. 76:11254-11264.
16. Froshauer, S., J. Kartenbeck, and A. Helenius. 1988. Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. J. Cell Biol. 107:2075-2086.
17. Garmashova, N., R. Gorchakov, E. Frolova, and I. Frolov. 2006. Sindbis virus nonstructural protein nsP2 is cytotoxic and inhibits cellular transcription. J. Virol. 80:5686-5696.
18. Garmashova, N., R. Gorchakov, E. Volkova, S. Paessler, E. Frolova, and I. Frolov. 2007. The Old World and New World alphaviruses use different virus-specific proteins for induction of transcriptional shutoff. J. Virol. 81:2472-2484.
19. Gorchakov, R., E. Frolova, S. Sawicki, S. Atasheva, D. Sawicki, and I. Frolov. 2008. A new role for ns polyprotein cleavage in Sindbis virus replication. J. Virol. 82:6218-6231.
20. Gorchakov, R., E. Frolova, B. R. Williams, C. M. Rice, and I. Frolov. 2004. PKR-dependent and -independent mechanisms are involved in translational shutoff during Sindbis virus infection. J. Virol. 78:8455-8467.
21. Griffin, D. E. 2001. Alphaviruses, p. 917-962. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4rth ed. Lippincott, Williams and Wilkins, New York, NY.
22. Grimley, P. M., I. K. Berezesky, and R. M. Friedman. 1968. Cytoplasmic structures associated with an arbovirus infection: loci of viral ribonucleic acid synthesis. J. Virol. 2:1326-1338.
23. Grimley, P. M., J. G. Levin, I. K. Berezesky, and R. M. Friedman. 1972. Specific membranous structures associated with the replication of group A arboviruses. J. Virol. 10:492-503.
24. - temperature-sensitive mutants of Sindbis virus: complementation group F mutants have lesions in nsP4. J. Virol. 63:1194-1202.
25. Hardy, W. R., and J. H. Strauss. 1989. Processing the nonstructural proteins of Sindbis virus: nonstructural proteinase is in the C-terminal half of nsP2 and functions both in cis and trans. J. Virol. 63:4653-4664.
26. Irvine, K., R. Stirling, D. Hume, and D. Kennedy. 2004. Rasputin, more promiscuous than ever: a review of G3BP. Int. J. Dev. Biol. 48:1065-1077.
27. Johnston, R. E., and C. J. Peters. 1996. Alphaviruses, p. 843-898. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Virology, 3rd ed. Lippincott-Raven, New York, NY.
28. Katsafanas, G. C., and B. Moss. 2007. Colocalization of transcription and translation within cytoplasmic poxvirus factories coordinates viral expression and subjugates host functions. Cell Host Microbe 2:221-228.
29. Kedersha, N., and P. Anderson. 2007. Mammalian stress granules and processing bodies. Methods Enzymol. 431:61-81.
30. Kedersha, N., G. Stoecklin, M. Ayodele, P. Yacono, J. Lykke-Andersen, M. J. Fritzler, D. Scheuner, R. J. Kaufman, D. E. Golan, and P. Anderson. 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169:871-884.
31. Kinney, R. M., B. J. B. Johnson, J. B. Welch, K. R. Tsuchiya, and D. W. Trent. 1989. The full-length nucleotide sequences of the virulent Trinidad donkey strain of Venezuelan equine encephalitis virus and its attenuated vaccine derivative, strain TC-83. Virology 170:19-30.
32. Kloks, C. P., C. A. Spronk, E. Lasonder, A. Hoffmann, G. W. Vuister, S. Grzesiek, and C. W. Hilbers. 2002. The solution structure and DNA-binding properties of the cold-shock domain of the human Y-box protein YB-1. J. Mol. Biol. 316:317-326.
33. Koonin, E. V., A. E. Gorbalenya, M. A. Purdy, M. N. Rozanov, G. R. Reyes, and D. W. Bradley. 1992. Computer-assisted assignment of functional domains in the nonstructural polyprotein of hepatitis E virus: delineation of an additional group of positive-strand RNA plant and animal viruses. Proc. Natl. Acad. Sci. USA 89:8259-8263.
34. Kujala, P., A. Ikaheimonen, N. Ehsani, H. Vihinen, P. Auvinen, and L. Kaariainen. 2001. Biogenesis of the Semliki Forest virus RNA replication complex. J. Virol. 75:3873-3884.
35. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
36. LaStarza, M. W., A. Grakoui, and C. M. Rice. 1994. Deletion and duplication mutations in the C-terminal nonconserved region of Sindbis virus: effects on phosphorylation and on virus replication in vertebrate and invertebrate cells. Virology 202:224-232.
37. LaStarza, M. W., J. A. Lemm, and C. M. Rice. 1994. Genetic analysis of the nsP3 region of Sindbis virus: evidence for roles in minus-strand and subgenomic RNA synthesis. J. Virol. 68:5781-5791.
38. Lemm, J. A., R. K. Durbin, V. Stollar, and C. M. Rice. 1990. Mutations which alter the level or structure of nsP4 can affect the efficiency of Sindbis virus replication in a host-dependent manner. J. Virol. 64:3001-3011.
39. Lemm, J. A., and C. M. Rice. 1993. Roles of nonstructural polyproteins and cleavage products in regulating Sindbis virus RNA replication and transcription. J. Virol. 67:1916-1926.
40. Lemm, J. A., T. Rümenapf, E. G. Strauss, J. H. Strauss, and C. M. Rice. 1994. Polypeptide requirements for assembly of functional Sindbis virus replication complexes: a model for the temporal regulation of minus and plus-strand RNA synthesis. EMBO J. 13:2925-2934.
41. Leon, C. A. 1975. Sequelae of Venezuelan equine encephalitis in humans: a four year follow-up. Int. J. Epidemiol. 4:131-140.
42. Li, G., M. W. LaStarza, W. R. Hardy, J. H. Strauss, and C. M. Rice. 1990. Phosphorylation of Sindbis virus nsP3 in vivo and in vitro. Virology 179:416-427.
43. Liljeström, P., S. Lusa, D. Huylebroeck, and H. Garoff. 1991. In vitro mutagenesis of a full-length cDNA clone of Semliki Forest virus: the small 6,000-molecular-weight membrane protein modulates virus release. J. Virol. 65:4107-4113.
44. Lowthert, L. A., N. O. Ku, J. Liao, P. A. Coulombe, and M. B. Omary. 1995. Empigen BB: a useful detergent for solubilization and biochemical analysis of keratins. Biochem. Biophys. Res. Commun. 206:370-379.
45. Lu, Z. H., J. T. Books, and T. J. Ley. 2006. Cold shock domain family members YB-1 and MSY4 share essential functions during murine embryogenesis. Mol. Cell. Biol. 26:8410-8417.
46. Lu, Z. H., J. T. Books, and T. J. Ley. 2005. YB-1 is important for late-stage embryonic development, optimal cellular stress responses, and the prevention of premature senescence. Mol. Cell. Biol. 25:4625-4637.
47. McInerney, G. M., N. L. Kedersha, R. J. Kaufman, P. Anderson, and P. Liljestrom. 2005. Importance of eIF2α phosphorylation and stress granule assembly in alphavirus translation regulation. Mol. Biol. Cell 16:3753-3763.
48. Michel, G., O. Petrakova, S. Atasheva, and I. Frolov. 2007. Adaptation of Venezuelan equine encephalitis virus lacking 51-nt conserved sequence element to replication in mammalian and mosquito cells. Virology 362:475-487.
49. Paranjape, S. M., and E. Harris. 2007. Y box-binding protein-1 binds to the dengue virus 3′-untranslated region and mediates antiviral effects. J. Biol. Chem. 282:30497-30508.
50. Peranen, J., and L. Kaariainen. 1991. Biogenesis of type I cytopathic vacuoles in Semliki Forest virus-infected BHK cells. J. Virol. 65:1623-1627.
51. Peränen, J., M. Rikkonen, P. Liljeström, and L. Käariänen. 1990. Nuclear localization of Semliki Forest virus-specific nonstructural protein nsP2. J. Virol. 64:1888-1896.
52. Ranki, M., I. Ulmanen, and L. Kaariainen. 1979. Semliki Forest virus-specific nonstructural protein is associated with ribosomes. FEBS Lett. 108:299-302.
53. Rico-Hesse, R., S. C. Weaver, J. de Siger, G. Medina, and R. A. Salas. 1995. Emergence of a new epidemic/epizootic Venezuelan equine encephalitis virus in South America. Proc. Natl. Acad. Sci. USA 92:5278-5281.
54. Salonen, A., L. Vasiljeva, A. Merits, J. Magden, E. Jokitalo, and L. Kaariainen. 2003. Properly folded nonstructural polyprotein directs the Semliki Forest virus replication complex to the endosomal compartment. J. Virol. 77:1691-1702.
55. Serva, S., and P. D. Nagy. 2006. Proteomics analysis of the tombusvirus replicase: Hsp70 molecular chaperone is associated with the replicase and enhances viral RNA replication. J. Virol. 80:2162-2169.
56. Shaner, N. C., R. E. Campbell, P. A. Steinbach, B. N. Giepmans, A. E. Palmer, and R. Y. Tsien. 2004. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22:1567-1572.
57. Shirako, Y., and J. H. Strauss. 1994. Regulation of Sindbis virus RNA replication: uncleaved P123 and nsP4 function in minus strand RNA synthesis whereas cleaved products from P123 are required for efficient plus strand RNA synthesis. J. Virol. 185:1874-1885.
58. Strauss, E. G., C. M. Rice, and J. H. Strauss. 1984. Complete nucleotide sequence of the genomic RNA of Sindbis virus. Virology 133:92-110.
59. Strauss, J. H., and E. G. Strauss. 1994. The alphaviruses: gene expression, replication, evolution. Microbiol. Rev. 58:491-562.
60. Takkinen, K. 1986. Complete nucleotide sequence of the non-structural protein genes of Semliki Forest virus. Nucleic Acids Res. 14:5667-5682.
61. Vida, T. A., and S. D. Emr. 1995. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128:779-792.
62. Wang, Y. F., S. G. Sawicki, and D. L. Sawicki. 1994. Alphavirus nsP3 functions to form replication complexes transcribing negative-strand RNA. J. Virol. 68:6466-6475.
63. Weaver, S. C., and A. D. Barrett. 2004. Transmission cycles, host range, evolution and emergence of arboviral disease. Nat. Rev. Microbiol. 2:789-801.
64. Weaver, S. C., and I. Frolov. 2005. Togaviruses, p. 1010-1024. In B. W. J. Mahy and V. ter Meulen (ed.), Virology, vol. 2. ASM Press, Salisbury, United Kingdom.
65. Weaver, S. C., A. Hagenbaugh, L. A. Bellew, L. Gousset, V. Mallampalli, J. J. Holland, and T. W. Scott. 1994. Evolution of alphaviruses in the eastern equine encephalomyelitis complex. J. Virol. 68:158-169.
66. Weaver, S. C., R. Salas, R. Rico-Hesse, G. V. Ludwig, M. S. Oberste, J. Boshell, R. B. Tesh, et al. 1996. Re-emergence of epidemic Venezuelan equine encephalomyelitis in South America. Lancet 348:436-440.
67. Zarate, S., M. A. Cuadras, R. Espinosa, P. Romero, K. O. Juarez, M. Camacho-Nuez, C. F. Arias, and S. Lopez. 2003. Interaction of rotaviruses with Hsc70 during cell entry is mediated by VP5. J. Virol. 77:7254-7260.